AProceedingsttraction of of P theest HMawaiianoths to E Fntomologicalloral Lures Society (2011) 43:49–58 49

Attraction of (: , ) to Floral Lures on the Island of

Peter Landolt1, Eric Jang2, Lori Carvalho2, and Michael Pogue3 1USDA, ARS, Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, Wapato, 98951 USA (corresponding author, [email protected]) 2USDA, ARS, PBARC, 64 Nowelo St., Hilo, Hawaii 96720, USA, [email protected] 3USDA, ARS, Systematic Entomology Laboratory, MRC-108, Smithsonian Institution, Washington DC 20013, USA, [email protected]

Abstract. Traps baited with floral chemicals on the island of Hawaii captured several pest species. eriosoma (Doubleday) (green garden looper), Au- tographa biloba (Doubleday) (bi-lobed looper), and unipuncta (Haworth) (true armyworm), all Noctuidae, as well as Hymenia recurvalis (L.) (beet webworm), a Crambidae, were trapped with (PAA). There was no response by moths to β-myrcene (BM), methyl salicylate (MS), cis jasmone (CJ), methyl-2-methoxy benzoate (MMB), 2-phenylethanol (2PE), or linalool (LIN) when these chemicals were tested singly. When other floral chemicals were presented in traps with PAA, numbers of C. eriosoma captured were increased by BM, MS, 2PE or MMB. Numbers of A. biloba and saucia (Hübner) (variegated cutworm) were increased by including BM with PAA in traps. Numbers of M. unipuncta were increased by BM or 2PE, and numbers of H. recurvalis were increased by MMB or LIN, presented with PAA. Both sexes of these five species of moths were trapped with floral lures, most females captured were mated, and many females possessed mature eggs.

Key Words: Crambidae, floral chemical, lure, Noctuidae, trap

Introduction Flowers of several species of plants are sources of chemical attractants that can be used to trap some pest moths. These flowers include Araujia sericiphera (bladderflower) (Cantelo and Jacobson 1979), Abelia grandiflora (glossy Abelia) (Haynes et al. 1991), Lonicera japonica (Japanese honeysuckle) (Pair and Horvat 1997), Cestrum nocturnum (night-blooming Jessamine) (Heath et al. 1992), Gaura spp (Shaver et al. 1997), Berberis aquifolium (Oregongrape) (Landolt and Smithhisler 2003), Buddleia davidii (butterfly bush) (Guédot et al. 2008), and (Canada thistle) (El-Sayed et al. 2008). Pest species of loopers in the noctuid subfamily are noteworthy in their strong attraction to floral compounds from these plants. Floral chemicals have been experimentally demonstrated as attractants for trapping ni (Hübner ) ( looper) (Landolt et al 2006), (Walker) ( looper) (Meagher 2002; Meagher and Landolt 2008), californica (Speyer) ( looper) (Landolt et al. 2001, 2006), Autographa gamma (L.) ( moth) (Molleman et al. 1997; Toth et al. 2010), falcifera (Kirby) ( looper) (Landolt et al. 2011), and orichalcea (F.) (old world soybean looper) (Stringer et al. 2008). Floral chemicals that attract pest Plusiinae include PAA, methyl salicylate (MS), methyl-2-methoxy benzoate (MMB), β-myrcene (BM), cis-jasmone (CJ), 2-phenylethanol (2PE), linalool (LIN), benzaldehyde, and benzyl alcohol (i.e., Cantelo and Jacobson 1979; Haynes et al. 1991; Heath et al. 1992; Landolt et al. 2001, 2006; Meagher and Landolt 2008, 2010; Molleman et al. 1997; Toth et al. 2010). 50 Landolt et al. These chemicals, and combinations thereof, are also attractive to several non-pest Plusiinae species such as confusa (Stephens) (Toth et al. 2010), and verruca (F.) and oxygramma (Geyer) (Meagher and Landolt 2008), and moths in other noctuid subfamilies and other families (Landolt et al. 2007, 2011; Lopez et al. 2000; Meagher and Landolt 2010; Toth et al. 2010). Plusiinae moth responses to flower chemicals have been demonstrated for a number of North American species, although related moth taxa in other geographic areas are likely to respond similarly to these chemicals. For example, Stringer et al. (2008) demonstrated attraction of T. orichalsea to volatiles of flowers of Canada thistle in . (Doubleday), a plusiine noctuid referred to as the green garden looper, is widely distributed in the Orient (Konenko and Pinratana 2005) and has a broad host plant range, attacking numerous vegetable and forage (Holloway 1985). Its distribution includes the Hawaiian Islands, where it is an introduced pest of vegetables (Luther et al. 1996). We took advantage of C. eriosoma occurrence in an agricultural area on the island of Hawaii to determine if it is attracted to floral chemicals that are lures for other pestiferous Plusiinae. We were particularly interested to determine C. eriosoma responses to these chemicals because of the strong attraction to floral chemicals by the closely related C. includens of North and Central America (Meagher 2001; Meagher and Landolt 2008). Additional information was obtained and is here reported on the capture of several other noctuid moths and the beet webworm, Hymenia recurvalis (L.) (Crambidae) in traps baited with floral chemicals.

Materials and Methods Four field trapping experiments (referred to as A, B, C, and D) evaluated moth attraction to floral chemicals and their combinations on the island of Hawaii. These experiments compared moths trapped with (A) PAA, BM, and MS, (B) PAA, CJ, and methyl-2-methoxy benzoate (MMB), (C) PAA, 2PE, and LIN, and (D) a range of release rates of the combination of PAA and BM. All experiments were conducted in a vegetable growing region near Waimea, Hawaii. Traps were placed within mixed fields of (cabbage), Brassica alboglabra (turnip mustard), Brassica kali (Chinese kale), Raphanus sativa (radish), Lactuca sativa (), Cucurbita spp. (squash), and Cynara scolymus (artichoke). Universal Moth Traps (UniTraps, AgriSense, PontyPridd, UK) that were used for these experiments consisted of a white bucket covered by a yellow cone and a green lid. A 2.2 cm2 piece of Vaportape® (Hercon Environmental Inc., Emigsville, PA) was placed within the bucket to kill captured , and was replaced every 4 weeks. Traps were 10 m apart and were checked twice per week. Lures were 8 ml polypropylene vials (Nalge Nunc, Rochester, NY) with a 3 mm hole in the lid to provide release of volatilized chemicals. For each chemical tested, 4 ml of active ingredient were loaded onto cotton balls in the bottom of a vial as described by Landolt et al. (2001), and the vial was suspended within the inside of the trap bucket. For all four field tests, a randomized complete block design was used, with six block replicates. The first three experiments tested for evidence of moth attraction to each of the tested chemicals, and for interaction between PAA and the other chemicals. Test dates and lure chemicals for each test are provided in Table 1. Test D compared numbers of moths trapped over a range of release rates of PAA + BM. This chemical combination was used in this test because of its overall performance as a lure in test A. For all traps, PAA and BM were each loaded into separate 8 ml polypropylene vials, each at a dose of 4 ml per vial on cotton balls. The release rate was varied by the size of the hole in the lid of the vial. Trapping dates and treatments are provided in Table 1. A subset of female moths captured in test D was dissected to determine their status as indicated by the number of spermatophores in the bursa copulatrix, and numbers of eggs present. Moths were Attraction of Pest Moths to Floral Lures 51 scored for their reproductive state as (I) unmated and no mature eggs, (II) mated and with mature eggs, and stage III, mated and no eggs. For tests A, B, and C, trap captures for each PAA+MS PAA+MMB PAA+LIN ------Treatment 5 Treatment species were analyzed and treatment means were separated by the Mann-Whitney Test (DataMost 1995). For test D, trap catch data were analyzed by a one-way ANOVA testing for effect of vial hole diameter on mean numbers of moths trapped. Within a species, and for female and male H. MS MMB LIN 12.0 mm recurvalis, means were separated using Tukey’s test at p < 0.05. Treatment 4 Treatment Voucher specimens of moth species trapped are deposited in the James Entomological Collection, Washington State University, Pullman, WA. We follow Lafontaine and Schmidt (2010) on the of . PAA+BM PAA+CJ PAA+2PE 6.0 mm Treatment 3 Treatment Results Test A. Numbers of C. eriosoma captured were significantly greater in traps baited with PAA+ BM and PAA + MS, compared to unbaited traps (Table 2). We interpret such responses to be BM CJ 2PE 3.0 mm evidence of attraction to trap lures. Autographa Treatment 2 Treatment biloba (Doubleday) moths were most frequently captured in traps baited with PAA + BM, and numbers of these moths in PAA+BM traps were significantly greater than in unbaited traps.

Mythimna unipuncta (Haworth) (true armyworm) PAA PAA PAA 1.5 mm moths were attracted to PAA, and the inclusion

Treatment 1 Treatment of BM significantly increased their numbers in traps. Hymenia recurvalis (L.) (beet webworm) moths were attracted to PAA, and inclusion of BM or MS with PAA did not significantly enhance No lure No lure No lure No lure their response over PAA alone (Table 2). The Control numbers of H. recurvalis moths trapped were much higher than the numbers of C. eriosoma or other noctuids captured. Totals of 22 C. eriosoma, 33 M. unipuncta, 20 A. biloba, and 466 female and 655 male H. recurvalis were captured in this test. Test B. Numbers of C. eriosoma trapped were

Dates significantly greater in traps baited with PAA compared to unbaited traps (Table 3). moths were captured in traps baited with 18 March to 14 April 18 March to 14 15 April to 31 May 15 15 April to 31 May 15 3 June to 7 July PAA, but other chemicals tested were not attractive

Trap Trap baits for field experiment A, B, C, testing β-myrcene (BM), cis jasmone (CJ), linalool (LIN), methyl-2-methoxy benzoate (MMB), and did not increase M. unipuncta response to PAA. Hymenia recurvalis moths were attracted to PAA, and numbers trapped with PAA + MMB were greater than with PAA alone. Totals of 14 C. methyl salicylate (MS), 2-phenylethanol (2PE), and phenylacetaldehyde (PAA) alone compared to combinations of PAA and the other chemicals. Trap Trap chemicals. other the and PAA of combinations to compared alone (PAA) phenylacetaldehyde and (2PE), 2-phenylethanol (MS), salicylate methyl bait treatments for experiment D were different hole sizes in vials of providing a varied mixture release of rates PAA+BM, of the attractant. Waimea, Hawaii, 2011. Experiment Table Table 1. A B C D 52 Landolt et al. eriosoma, 18 M. unipuncta, and 278 female and 349 male H. recurvalis were captured in this test. Test C. PAA was attractive to C. eriosoma, although numbers of moths captured were lower than in the other tests (Table 4). 2PE and LIN did not enhance C. eriosoma response to PAA. Mythimna unipuncta moths were attracted to the combination of PAA + 2PE. Hymenia recurvalis 0.7 + 0.3 a 1.3 + 0.6 b 1.2 + 0.5 b PAA + MS PAA 47.0 + 7.2 b moths were attracted to PAA, and LIN increased 34.7 + 6.9 b their response to PAA. Totals of 10 C. eriosoma, 13 M. unipuncta, and 220 female and 163 male H. recurvalis, were captured in this test. When results for unbaited and PAA-baited traps from the three tests are combined, the C. eriosoma MS

response to PAA is highly significant by a paired 0.0 + 0.0 + a 0.2 + a 0.0 + a t-test (P = 0.002, t = 3.72, df = 17). Similarly, for 0.0 + a the three tests combined, numbers of A. biloba and M. unipuncta trapped with PAA were significantly greater than unbaited traps (p=0.03, t=2.37, df =17 for A. biloba; p=0.004, t=3.34, df=17 for M. unipuncta). 3.3 + 0.6 c 1.8 + 0.7 b Test D. Numbers of four pest noctuid moths [C. 2.0 + 0.5 b PAA + BM PAA 35.0 + 6.9 b 23.2 + 5.5 b eriosoma, A. biloba, M. unipuncta, and (Hübner)] were greater in traps baited with PAA + BM compared to unbaited traps (Figure 1a). Greatest numbers of C. eriosoma were captured with vials with a 6 mm diam hole in the lid. We at p < 0.05. Test, Whitney ferent by the Mann did not demonstrate a clear optimum hole diameter BM 0.2 + a 0.2 + a 0.0 + a (controlling chemical release) for A. biloba, M. 0.0 + a 0.2 + a unipuncta or P. saucia, but overall vials with a 6 mm diameter hole might be the best choice. For A. biloba, numbers of moths caught were greater for

6 mm diam vial holes, compared to 1.5 or 3 mm diam vial holes, and for M. unipuncta, numbers of moths caught were greater with 3, 6, or 12 mm PAA 0.5 + 0.2 a 0.7 + 0.3 a 0.8 + 0.3 b 19.5 + 6.0 b vial hole diameters compared to 1.5 mm diam 27.0 + 10.1 b holes. For P. saucia, there were no significant differences in numbers trapped between any vial hole diameters (Figure 1a). Numbers of H. recurvalis moths captured were similar for PAA + BM lures across all vial hole diameters tested Control 0.0 + a 0.0 + a 0.0 + a (Figure 1b). For male and female H. recurvalis, 0.0 + a 0.0 + a and for each vial hole diameter, nmbers of moths captured in baited traps were significantly greater than unbaited traps. Totals of 79 C. eriosoma, 35 ♂ A. biloba, 110 M. unipuncta, 47 P. saucia, and 441 ♀ female and 411 male H. recurvalis were captured in this test. Small numbers of other species of pest moths were captured in traps baited with floral chemicals Table 2 . Mean Table numbers of pest moth species captured in traps baited with β-myrcene phenylacetaldehyde (BM), (PAA), methyl salicylate (MS) and Hawaii. 2011. Waimea, combinations of those chemicals, Moth H. recurvalis H. recurvalis C. eriosoma A. biloba M. unipuncta Means within a row followed by the same letter are not significantly dif Attraction of Pest Moths to Floral Lures 53 0.5 + 0.3a 0.8 + 0.3b 1.0 + 0.4b 15.7 + 2.6c 23.2 + 4.1c 0.33 + 0.2a 33.0 + 4.3c 25.5 + 3.3c PAA + LIN PAA PAA + MMB PAA LIN MMB 0.0 + 0.0a 0.0 + 0.0a 0.0 + 0.0a 0.2 + 0.2a 0.8 + 0.4a 0.3 + 0.2a 0.0 + 0.0a 0.0 + 0.0a 0.7 + 0.3a 6.3 + 1.3b 8.2 + 1.2b 1.3 + 0.2b 1.0 + 0.4b PAA + CJ PAA 0.83 + 0.2b 10.8 + 1.4b 12.0 + 1.7b PAA + 2PE PAA ferent by the Mann Whitney Test, at p < 0.05. Test, Whitney ferent by the Mann ferent by the Mann Whitney Test, at p < 0.05. Test, Whitney ferent by the Mann CJ 2PE 0 + 0a 0.5 + 0.2a 0.0 + 0.0a 0.3 + 0.2a 0.8 + 0.5a 0.2 + 0.2a 0.0 + 0.0a 0.2 + 0.2a

PAA PAA 0.5 + 0.2a 0.0 + 0.0a 4.2 + 1.2b 5.0 + 0.9b 8.2 + 1.5b 0.8 + 0.3b 0.8 + 0.3b 12.0 + 1.5b Control Control 0.5 + 0.5a 0.2 + 0.2a 0.0 + 0.0a 0.0 + 0.0a 0.7 + 0.3a 0.2 + 0.2a 0.0 + 0.0a 0.0 + 0.0a ♂ ♀ ♂ ♀ H. recurvalis H. recurvalis C. eriosoma M. unipuncta Means within a row followed by the same letter are not significantly dif Mean numbers of pest moth species captured in traps baited with phenylacetaldehyde (PAA), 2-phenylethanol (2PE), and linalool (LIN), and (LIN), linalool and (2PE), 2-phenylethanol (PAA), phenylacetaldehyde with baited traps in captured species moth pest of numbers Mean 4. Table Hawaii. 2011. Waimea, combinations of those chemicals, Moth H. recurvalis H. recurvalis C. eriosoma M. unipuncta Means within a row followed by the same letter are not significantly dif . Mean numbers of pest moth species captured in traps baited with phenylacetaldehyde PAA), cis jasmone (CJ), and methyl-2-methoxy benzoate methyl-2-methoxy and (CJ), jasmone cis PAA), phenylacetaldehyde with baited traps in captured species moth pest of numbers Mean 3 . Table Hawaii. 2011. (MMB) and combinations of those chemicals.Waimea, Moth 54 Landolt et al.

Figure 1. Numbers of noctuid pests (A) and a crambid moth pest (B) captured in traps baited with phenylacetaldehyde and β-myrcene dispensed from vials. Vials were provided holes in the lids for volatile release, and several vial hole diameters were used to vary volatile release rates from the vials. For A, filled triangles are forC. eriosoma, filled circles are for A. biloba, open triangles are for M. unipuncta, and open squares are for P. saucia. For B, filled circles are for maleH. recurvalis and filled triangles are for femaleH. recurvalis. Attraction of Pest Moths to Floral Lures 55 in this study, but they were too few to be analyzed statistically. These included T. ni, Helicoverpa zea (Boddie) (the corn earworm), Feltia subterranea (F.) N 62 31 17 13 (subterranean cutworm), and Spodoptera mauritia 31 (Boisduval). Numbers of A. biloba captured were insufficient for statistical analyses in tests B and C, and numbers of P. saucia were insufficient for statistical analyses in tests A, B, and C. Both sexes of each of these moth species were captured in traps baited with these floral lures. For the 4 tests combined, we captured 82 female and 43

male C. eriosoma, 36 female and 30 male A. biloba, Hawaii. Waimea, 1.32 ± 0.08 2.74 ± 0.22 2.18 ± 0.31 1.84 ± 0.22 1.65 ± 0.18 56 female and 118 male M. unipuncta, 47 female Spermatophores and 23 male P. saucia, and 1404 female and 1578 male H. recurvalis moths. Most noctuids dissected were mated and had mature eggs, although smaller numbers were unmated or had no eggs (Table 5). Most H. recurvalis females were mated but were without eggs (Table 5). There were 1.6 ± 0.18 (n = 31) spermatophores per female C. eriosoma, 1.8 ± 0.22 (n 4 55 42 46 = 13) spermatophores per female A. biloba, 2.2 ± 0.31 36 (n = 17) spermatophores per female M. unipuncta, 2.7 ± 0.22 (n = 31) spermatophores per female P. saucia and 1.3 + 0.08 (n = 68) spermatophores per female

H. recurvalis. state III % Reproductive

Discussion Chrysodeixis eriosoma moths were attracted to PAA, but not to any other single-chemical lures that we 40 90 53 54 tested. The lack of statistically significant differences 52 between numbers of this species trapped with PAA versus unbaited traps in tests A and C may have been due to overall low numbers of moths present. The chemicals BM, 2PE, MS, and MMB, when presented state II % Reproductive with PAA, enhanced C. eriosoma moth response over PAA alone. Stringer et al. (2008) in New Zealand captured 91 C. eriosoma moths (64 female, 27 male) in traps baited with floral chemicals but did not provide information on which compounds they responded to 5 6 5 0 or statistical support for C. eriosoma responses to 13 lures. We are not aware of other reports of feeding attractants or lures for females of this species. This is the first experimental demonstration then of attraction of C. eriosoma to floral chemicals and confirms the state I % Reproductive observation of Stringer et al (2008) who trapped the moth with floral chemicals. We do not yet know if these lures are attractive enough to be of practical use in monitoring or managing pest populations of C. eriosoma. A female-produced sex that H. recurvalis P. saucia P. M. unipuncta Female reproductive state and female mating frequency for moths captured in floral lure traps. Reproductive state I is unmated, II is mated and mated is II unmated, is I state Reproductive traps. lure floral in captured moths for frequency mating female and state reproductive Female 5. Table with mature eggs, and III is mated no eggs. Mating frequency was determined as spermatophores per female. Moth species A. biloba C. eriosoma 56 Landolt et al. is attractive to C. eriosoma males was identified by Benn et al. (1982), and its field activity was confirmed by Hai et al. (2002). The soybean looper moth, C. includens, is a close relative of C. eriosoma, and is also attracted to PAA. Like C. eriosoma, C. includens responded more strongly to traps baited with PAA + BM versus PAA alone, but unlike C. eriosoma, C. includens has not shown a statistically significant enhanced response to combinations of PAA with 2PE, MS, or MMB compared to PAA alone (Meagher and Landolt 2008). However, in that study (Meagher and Landolt 2008), numbers of C. includens trapped with PAA + MS and PAA + MMB were 76% and 60% higher respectively compared to PAA. Chrysodeixis eriosoma, unlike C. includens in (Meagher and Landolt 2008), did not show an enhanced response to PAA + CJ versus PAA. Further experimentation is needed to further clarify the relative responses of C. includens, C. eriosoma, and other looper species to various floral chemicals and combinations thereof. A second species of Plusiinae, A. biloba, was attracted to PAA in this study, and like C. eriosoma, more A. biloba moths were trapped when BM was added with PAA. This is the first report ofA. biloba attraction to floral chemical lures.Autographa biloba is not generally considered a pest species, but is polyphagous and has been found on plants (Canerday and Arant 1966). The captures of an armyworm (M. unipuncta) and a cutworm (P. saucia) species in the traps was unexpected, although moths in noctuid moth taxa other than Plusiinae are reported to be attracted to floral volatiles (Cantelo and Jacobson 1979, Toth et al. 2010, Landolt et al. 2011). Mythimna unipuncta is also attracted to the combination of acetic acid and 3-methyl-1-butanol, possibly as a feeding attractant (Landolt and Higbee 2002, Landolt et al. 2011). Interestingly, M. unipuncta was not trapped with a mixture of PAA, MS, MMB and BM during a field study comparing that floral lure with acetic acid plus 3-methyl-1- butanol (Landolt et al. 2011). This is a first report of P. saucia (Noctuinae) response to a floral lure. Small numbers of P. saucia were captured in traps baited with acetic acid plus 3-methyl-1-butanol by Landolt et al. (2011). The beet webworm H. recurvalis, in the family Crambidae, was also trapped with PAA and not with other chemicals tested singly. MMB and LIN enhanced H. recurvalis attraction to PAA. This is the first experimental demonstration of H. recurvalis attraction to PAA or any other floral chemicals. Creighton et al. (1973) captured 21H. recurvalis moths in traps baited with the combination of the sex pheromone of T. ni and PAA, and it is likely that H. recurvalis in that study responded to PAA and not to the T. ni sex pheromone. Several other species of Crambidae have been trapped with flower chemical lures. Meagher and Landolt (2008) captured Diaphania nitidalis Stoll (pickleworm), with the combinations of PAA plus CJ, LIN, MS, MMB or BM. Landolt et al. (2011) trapped the crambids rantalis (Guenée), Petrophila avernalis (Grote), and profundalis (Packard) with a mixture of PAA, MS, MMB, and BM. The numbers of C. eriosoma, A. biloba, and M. unipuncta captured were consistently low compared to responses to floral chemicals obtained for some noctuid moths in other studies, such as C. includens in Florida (Meagher and Landolt 2008), and A. californica in Washington (Landolt et al. 2001, 2006). Possible explanations are low population densities of the moths in these vegetable fields, a relatively low rate of response of moths to the lures, and competition between lures and other natural odor sources or abundant food sources. Studies relating the trapping of moths with feeding attractant lures and other measures of moth abundance are generally lacking. All of these moths can be pests of agricultural crops. There may be potential to develop these attractants as a means of monitoring pest species in crops, or to develop attract-and- kill methods for population suppression. The trap response of female as well as male moths Attraction of Pest Moths to Floral Lures 57 and the inclusion of females with eggs in trap catches suggest a potential to use these types of lures in an attract-and-kill approach to remove female moths and reduce oviposition on crop plants. Preliminary work to develop such an approach has been conducted with PAA to lure T. ni moths to a pesticide-treated food bait (Landolt et al. 1991) and to use PAA with BM to lure A. californica moths to a pesticide-treated visual target (Camelo et al. 2007).

Acknowledgments Technical assistance was provided by D. Green and J. Brumley. T. S. Davis assisted with statistical analysis of data. We thank Ken Hufford and Paul Johnston for access to their vegetable farms.

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